Similar and dissociable mechanisms for attention to internalversus external information

Jennifer K RothMagnetic Resonance Research Center, Department of Diagnostic Radiology, Yale School ofMedicine, 300 Cedar St, New Haven, CT, 06520-8043

Marcia K JohnsonDepartment of Psychology, Yale University, Box 208205, New Haven, CT. 06520-8205.marcia.johnson@yale.edu

Carol L RayeDepartment of Psychology, Yale University, Box 208205, New Haven, CT. 06520-8205.carol.raye@yale.edu

R Todd ConstableDepartments of Biomedical Engineering, and Neurosurgery, Director MRI Research, co-DirectorYale MRRC, Yale University School of Medicine, 300 Cedar Street, PO Box 208043, New Haven,CT 06520-8043 todd.constable@yale.edu

AbstractWe compared two attentional executive processes: updating, which involved attending to aperceptually-present stimulus, and refreshing, which involved attending to a mentally activerepresentation of a stimulus no longer perceptually present. In separate blocks, participants eitherreplaced a word being held in working memory with a different word (update), or they thought backto a just previously seen word that was no longer perceptually present (refresh). Bilateral areas offrontal cortex, supplementary motor area, and parietal cortex were similarly active for both updatingand refreshing, suggesting a common network of areas are recruited to bring information to the currentfocus of attention. In a direct comparison of update and refresh, regions more active for update thanrefresh included regions primarily in right frontal cortex, as well as bilateral posterior visualprocessing regions. Regions more active for refresh than update included regions primarily in leftdorsolateral frontal and left temporal cortex and bilateral inferior frontal cortex. These findings helpaccount for the similarity in areas activated across different cognitive tasks and may help specify theparticular executive processes engaged in more complex tasks.

Keywordsworking memory; update; refresh; maintenance

© 2009 Elsevier Inc. All rights reservedCorresponding author: Jennifer K Roth, Magnetic Resonance Research Center, Department of Diagnostic Radiology, Yale School ofMedicine, 300 Cedar St, New Haven, CT, 06520-8043 office: 203-737-5995, fax: 203-785- 6534, Jennifer.Roth@yale.edu.Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customerswe are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resultingproof before it is published in its final citable form. Please note that during the production process errors may be discovered which couldaffect the content, and all legal disclaimers that apply to the journal pertain.

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Published in final edited form as:Neuroimage. 2009 November 15; 48(3): 601–608. doi:10.1016/j.neuroimage.2009.07.002.

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IntroductionA common fronto-parietal network of areas (lateral prefrontal cortex, parietal cortex andsupplementary motor area) is active in many cognitive tasks (Cabeza and Nyberg, 2000;Duncan and Owen, 2000) including working memory (WM), visual attention (Kelley et al.,2008; Serences et al., 2005, 2007; Marois et al., 2003), and encoding (Blumenfeld andRanganath, 2007) and retrieval from long term memory (Cabeza et al., 2008). This similarityof activity is consistent with the idea that common component processes are recruited fordiverse cognitive tasks (Duncan and Owen, 2000; Cabeza and Nyberg, 2000; Johnson andHirst, 1993; see also Awh and Jonides, 2001; Awh, Vogel and Oh 2006). Characterizing thesecomponents more specifically is a major challenge for cognitive science.

Two component executive processes that might, in part, account for this common activationacross experiments are updating (Roth, Serences and Courtney, 2006) and refreshing (Johnsonet al., 2005). Updating, the replacement of an item actively being maintained in workingmemory with a different item, produces activity in a network including left inferior frontaljunction (IFJ, the junction of inferior frontal sulcus and inferior precentral sulcus), dorsolateralprefrontal cortex (DLPFC), supplementary motor area (SMA), and bilateral parietal cortexincluding intraparietal sulcus (IPS). This network becomes active during updating of differenttypes of visual stimuli (Roth et al., 2006), updating from a sensory stimulus or an item fromlong term memory (Roth and Courtney, 2007), and when the rule operating on a stimulus isupdated (Montojo and Courtney, 2008). Refreshing is the process of attending to informationthat is not perceptually present but is momentarily active from either recent perception orthought (e.g., thinking back to a just-seen stimulus no longer on the screen; Raye et al.,2002; Johnson et al., 2002, 2005). Refreshing produces activity in a network including DLPFC,anterior cingulate cortex (ACC), supramarginal gyrus (SMG), IPS, and middle temporal gyrus,for a variety of types of stimuli (Johnson et al., 2005; Raye et al, 2002, 2007).

Similarities in activation for updating and refreshing across experiments have been notedbefore (Courtney et al., 2007), but this is the first experiment to directly compare them. Onepossibility is that updating and refreshing are the same process investigated in the context ofdifferent experimental paradigms and under different names. If so, we would expect refreshingand updating to produce the same patterns of activation in the same participants in proceduresusing the same materials. On the other hand, Updating has been proposed as a specificmechanism for changing the contents of what is being actively maintained in working memoryby prioritizing new information that is concurrently perceived or retrieved. Refreshing has beenproposed as a general mechanism for briefly bringing information that is currently active butnot perceptually present to the foreground of attention. Update and refresh may involvedifferent areas of cortex. For example, Updating should show relatively greater activity inposterior visual processing regions as a new target is perceptually attended, and Refreshingshould show relatively greater activity in frontal regions (e.g., left DLPFC) associated withmodulating representations of no longer present perceptual stimuli (M.R. Johnson et al.,2007).

Assuming that there is a distinction between the cognitive operations and neural activityinvolved in perceptual vs. reflective attention (e.g., Dobbins & Han, 2006; Gilbert, Frith andBurgess, 2005; Johnson, Raye, Mitchell et al., 2005; Johnson & M.R. Johnson, in press),directly comparing the neural correlates of updating working memory from a perceptuallypresent stimulus with refreshing an active representation of a stimulus that is no longerperceptually present should help clarify similarities and differences in neural activity observedin more complex cognitive tasks that recruit these processes.

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MethodsParticipants

Participants were 22 (12 females) healthy adult (M = 24 yrs, range 19-44) non-smokers, withno history of head injury, psychiatric illness, drug or alcohol abuse, and no current medicationsthat would affect the function of the brain, heart or blood circulation. Participants werecompensated and all gave written informed consent. The experiments were undertaken withthe approval of Yale University School of Medicine Human Investigation Committee, and incompliance with national legislation and the Code of Ethical Principles for Medical ResearchInvolving Human Subjects of the World Medical Association.

ProcedureImmediately before the fMRI scan, participants had a practice session. They read taskinstructions, listened to verbal instructions, and performed one practice block of each condition(update, refresh) with experimenter feedback. They then performed, in random order, threeblocks of each condition without feedback (performance was monitored to determine that theywere doing the task correctly). Each practice block was 64.5 seconds.

There were 6 fMRI experimental runs. Within each run there were 4 blocks of each type (Updateand Refresh), presented pseudorandomly and counterbalanced within run and across scansession.

Task blocks were nearly identical in task set-up. Different geometric shapes were used as cuesfor Update (triangles), Refresh (circles) and Control (squares) conditions. Otherwise thestimulus presentation was the same. In both Update and Refresh blocks, words appeared onthe screen one at a time and participants were instructed to read them silently.

Update Blocks—In Update Blocks, there were four event types: read (words that did notmatch the word currently maintained in WM), update WM, match, and control. Participantswere given a word to maintain in WM and sometimes were cued (with a row of triangles) toreplace the word currently being held in WM with the next word to appear on the screen(update; see Figure 1). Thus, in Update blocks, participants always maintained one word asthe sample stimulus in WM while reading other words, and their task was to determine whethereach word they read matched or did not match the word being maintained. If the word on thescreen matched the item in WM, participants responded with a button press (match).Occasionally they saw a row of squares, a “null” cue acting as a sensory control event(control), and they were instructed to look at the squares, but continue to maintain the currentsample in WM and wait for the next word. Participants were to press a button only when theitem on the screen matched the contents of working memory (match).

Refresh Blocks—As in Update Blocks, single words appeared on the screen one at a timeand participants were instructed to read them. Within Refresh Blocks, there were four eventtypes: read, refresh, control, and match. During Refresh blocks participants performed amodified version of a refresh task (see Figure 1; Raye et al, 2002). Occasionally, instead of aword, they saw a row of dots which cued participants to think back to the word that precededthe refresh cue (refresh event). They were instructed to think back to that word once, and notcontinue to think of it. Occasionally they saw a row of squares that cued them to look at thesquares and wait for the next word; this served as a sensory control event in which they saw arow of geometric stimuli, as on Refresh trials, but were not asked to refresh. Occasionallyparticipants read a word they had recently refreshed; these `match' events were included toparallel match events in update trials. Read events corresponded to read trials from the non-

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match (read) trials in Update Blocks. Participants were not required to make any button pressresponses during the Refresh Blocks.

Stimulus Presentation—Before each block, a cue (“UPDATE” or “REFRESH”) appearedfor 1 second (Figure 1). Within each block, events occurred pseudorandomly with an Update(or Refresh) cue every 3 - 20 seconds (mean time between cues was 10.5 seconds). All eventswere counterbalanced such that each event type preceded and followed every other event typeequally often. Each word or cue appeared on the screen for 1 second with a 500 ms interstimulusinterval containing a visual mask (row of plus signs) that appeared between each word or cue.The row of plus signs subtended the same visual angle as the longest word. During the practicesession stimuli were presented on a Dell Inspiron 640m laptop running EPrime softwareVersion 1.1 (Psychology Software Tools), which also collected key press responses for matchevents in the Update blocks. During the fMRI session, stimuli were projected onto a screenlocated behind the participant's head inside the bore of the scanner. Participants viewed thestimuli via an angled mirror mounted on the head coil. Responses were collected via an MRI-compatible button box.

Stimuli were 24 repeated, 2- and 3-syllable abstract nouns (e.g., method, concept, quality,miracle). Each word appeared in 28-point Arial font centered on the screen in black lower-case font on a white background. In a pilot experiment, 23 participants evaluated words forimagability and emotionality on a 10 point rating scale. Words were eliminated whose scoreson either rating were more than two standard deviations from the mean on either measure.

The 6 fMRI experimental runs each lasted 9 minutes 18 seconds, for a total of 55 minutes, 48seconds of functional data collection. Each block lasted 64.5 seconds with a temporally jitteredinterblock interval where a row of pluses remained on the screen for 3-7.5 seconds. Across allscans there were 144 events of each type (update, refresh, read during the update task, readduring the refresh task, match in the update task, match in the refresh task).

fMRI Data Acquisition—All scans were collected on a Siemens 3T Trio scanner at theMagnetic Resonance Research Center, Yale University School of Medicine. Functional datawere collected as T2*-weighted gradient echo, echo planar images (TR = 2000 ms, TE = 25ms, Flip Angle = 80 degrees, voxel size 3.438 × 3.438 mm, 3 mm axial slice, 1 mm gap, FOV= 22cm, matrix = 64 × 64) during the experimental task. A high-resolution T1-weightedanatomical scan was collected between the 3rd and 4th functional scan runs (TR = 2530 ms,TE = 3.34, Flip Angle = 7 degrees; FOV = 256 × 256).

fMRI Analysis—Data were slicetime corrected and motion corrected with SPM5 as astandard lab preprocessing step. SPM software was not utilized after this point. Functional datawere filtered with a 3rd order polynomial orthogonal function to correct for mean, linear driftand any third order nuisance variable. The frequency of change between block types is morefrequent than the periodicity of a third order polynomial function, therefore this filter shouldnot reduce statistical power. Anatomical and functional images were coregistered thenmorphed into MNI space using BioimageSuite software (http://www.bioimagesuite.org). Afterpreprocessing, fMRI data were analyzed using Analysis of Functional NeuroImages (AFNI)software (Cox, 1996). Data were normalized to have a mean of 100. Data for each voxel wereanalyzed via a simultaneous regression for all critical and control events (Update, Read inUpdate, Match in Update, errors detecting match events, Control in Update, Refresh, Read inRefresh, Match in Refresh, Control in Refresh, Update and Refresh Block cues) as well asblock regressors for each block type (Update Block and Refresh Block). This was a mixedblock/event-related design. Each event included two stimuli. For example, an Update eventincluded the cue to update and the subsequent word to be maintained in working memory. Foreach event, the convolution of event regressors began with the onset of the first stimulus. Event

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regressors and block regressors both were convolved with a standard hemodynamic responsefunction using the AFNI software waver program (delay time = 2 seconds, rise time = 3 seconds,fall time = 5 seconds, no undershoot; Cox et al., 1996). Block regressors modeled sustainedactivity within the two block types. Simultaneous regression with the block regressors and theevent regressors allows for both sustained and transient components of the activity to beidentified (Visscher et al., 2003). Given the temporal jitter of events within blocks, thecorrelation between block and each event regressor did not exceed .3, allowing for an efficientestimation of sustained and event related activity. Interblock intervals were not modeled andcontributed to the baseline.

For the purpose of creating regressors for the different event types, all events modeled in thefMRI analysis included two successive stimuli. An update event included the update cue andthe subsequent word to be encoded into memory. Refresh events included the word to berefreshed (the just-previous item) and the refresh cue. Control events were modeled separatelywithin update and refresh blocks. In each case, an “event” included two stimuli. In the Updateblocks control events consisted of the control cue and subsequent word to be read, and inRefresh blocks, control events consisted of the control cue and the word preceding it. Readevents, modeled separately within update and refresh blocks, included two words in a row tobe read, that neither matched the contents of WM, each other, or the word recently refreshed.Match events included the item that matched the contents of WM and the subsequent word tobe read. Each of these events included two successive stimuli for the purpose of makingparticular direct comparisons. Within the update blocks direct comparisons were made betweenUpdate events and control events. An Update event included the cue to update and thesubsequent word, which was to be brought to the current focus of attention and maintained inworking memory; the control event included a null cue and a word to be read. The refresh eventincluded a word to be read followed by the cue to refresh; thus, its control event included aword to be read followed by a “null” cue. For direct comparisons between update and refresh,in both cases, the item to be brought into the current focus of attention was the second stimulusof a two stimulus event. Block cue events included the instructional cue marking the beginningof the block and the subsequent fixation cue. The block cue event only included one stimulusand was included simply to account for the variance in signal associated with this cue.

Individual participant data were smoothed with a three dimensional 4mm Gaussian kernel, thenentered into a series of t-tests to compare events of interest, with participant as a random factor.To find regions of the brain differentially active for each condition, t-tests compared thefollowing events: Update versus Control event within the Update blocks, Refresh versusControl event within the Refresh blocks, Update versus Refresh events, and Update Blockversus Refresh Block. This last comparison of activity for the Update Block versus RefreshBlock identified areas associated with sustained activity associated with WM maintenancesince maintenance was required in Update, but not Refresh, blocks.

For each resulting t-map, individual voxel thresholds were set at p < 0.01. Voxelwise data werecorrected for multiple comparisons by spatial extent of contiguous suprathreshold individualvoxels (experiment-wise p < 0.01 for a cluster). A Monte Carlo simulation was run in the AFNIsoftware package on a brain mask with 4x4x4 mm voxels, a smoothing kernel of 4 mm,connection radius of 5.2 mm, to determine that a 704 microlitre cluster satisfied a threshold ofp<0.01 (Forman et al, 1995).

To find regions of the brain similarly active in Update events, Refresh events, and sustainedmaintenance, we performed an overlap analysis of three Voxelwise t-maps: Update versusControl Events, Refresh versus Control Events, and Update blocks versus Refresh Blocks. Anoverlap map was generated using AFNI software by weighting equally the active voxels fromeach input map and summing the inputs to yield a map where different sums corresponded to

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different combinations of active conditions from the input maps. The threshold for each of thethree t-maps contributing to this overlap map was p < .01. Therefore, this is a conservativemethod for determining areas of overlap as each region of overlap must pass the threshold oftwo or more t-tests.

ResultsBehavioral results

The percent correct (87.3%, standard error 2.5%) for the response to match to sample, and falsealarm rate (0.17%, standard error 0.03%), in the Update task indicated that participantseffectively updated WM.

fMRI resultsOverlap in executive function areas—Figure 2 shows areas of activation associated withtransient activity associated with update and refresh, sustained activity associated with workingmemory maintenance (identified with a sustained block regressor for the Update blocks) andtheir overlap. As is clear from Figure 2, update and refresh both (red areas) showed activity inbilateral areas of precentral gyrus and superior frontal junction (SFJ) including left IFJ, rightmiddle frontal gyrus, SMA, bilateral inferior parietal lobule (IPL) and intraparietal sulcus(IPS), and an area of left posterior fusiform gyrus. Regions of left superior parietal cortex andright SMA were active for both update and maintenance (green areas). (See Table 1;supplementary Table 1 includes a complete list of regions for different combinations ofoverlap.)

Direct comparison of Update and Refresh—Areas more active for Update than Refreshevents included right SFJ and superior frontal sulcus, right superior and middle frontal gyrus,and bilateral primary and secondary visual cortex, and cuneus (see Figure 3, orange areas, andTable 1).

Regions more active for Refresh than Update events included left DLPFC (superior and middlefrontal gyrus), bilateral inferior frontal gyrus (including left IFJ), anterior insula, SMA, andACC, left IPL and left supramarginal gyrus, and left middle and superior temporal gyrus, (seeFigure 3, purple areas, and Table 1).

DiscussionThis study investigated two types of executive function: attending to a perceptual stimulus inorder to replace a representation in WM (update) and attending to an active representation thatis no longer perceptually present (refresh). We identified areas that were commonly activeacross these two types of executive function and areas that differed between these two executivefunctions.

Common regions of activation across types of executive functionIn the present experiment, both updating and refreshing brought information into the focus ofattention, either perceptually (update) or reflectively (refresh). For both processes, we foundanatomical areas similar to those found in other experiments involving attending to informationin various ways. For example, some areas in the current study that showed activity in bothupdate and refresh, including left precentral gyrus, IFJ, SMA, and bilateral IPS and IPL, aresimilar to those involved in visual attention switching (Serences et al, 2004), task switching(Derrfuss et al., 2005), episodic and semantic long-term memory retrieval (Shannon andBuckner, 2004; Nyberg et al, 2003), and to cues signaling the start of a task block (Dosenbachet al, 2006).

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A recent study also examined regions of activation common across tasks involving bringinginformation into the focus of attention (Marklund et al, 2007). They directly compared transientactivity during episodic and semantic long term memory and working memory to the transientactivity during an attention task. Aside from ACC/preSMA (SMA in the current study), theregions common to Update and Refresh in our study, as would be expected, were notdifferentially active across the memory and attention conditions in the Marklund et al. study.If, as we argue, Update and Refresh are both involved in bringing information to the focus ofattention, then we might expect that these common regions will be absent from comparisonswhere both conditions include such attentional processes.

Distinguishing elements of executive functionAlthough the commonality of activity across refreshing and updating was striking, equallyimportant are the differences we observed. First, Figure 2 shows that some areas exhibit afunctional topography where immediately adjacent regions were responsive to differentprocesses. For example in left superior parietal cortex, a region with diverse cell types,functional activity, and extensive connectivity to diverse regions (Rushworth, Behrens andJohansen-Berg, 2005; Nickel and Seitz, 2005;Scheperjans et al. 2008), there were adjacentregions showing activity for maintenance, both update and maintenance, update and refresh,and update. Similarly, different subregions were responsive to different elements of executivefunction in left IFJ and SMA.

A recent study by Dosenbach et al. (2006) also was directed at identifying common and distinctregions associated with executive functions. They compared 10 studies all conducted on thesame scanner, and all using a mixed blocked/event-related design, and various types ofcognitive tasks and materials. Comparing activations across studies, Dorsenbach et al.(2006) identified regions of dorsal anterior cingulate cortex/medial superior frontal cortex(Talairach coordinates -1, 10, 46), and bilateral anterior insula (-35, 14, 5; 36, 16, 4) commonacross tasks and phases within tasks. They suggested that these regions form a core task-setsystem. Consistent with this idea of a general purpose task-set system, we found an area ofSMA activation (see Supplementarly Table 1) in the overlap of Update, Refresh, andMaintenance within 2.5 voxels of their dorsal anterior cingulate cortex/medial superior frontalcortex area. Interestingly, in the Refresh condition, three areas (bilateral SMA/ACC, and leftand right anterior insula, see Supplementary Table 1) were within 7.3, 3 and 4.6 millimeters,respectively, of the three regions in Dosenbach et al.'s proposed core task set system. Thesefindings suggest that refreshing may be a component of the kind of core task set systemsuggested by Dosenbach et al. In addition, both studies suggest there may be more functionalspecificity within areas commonly reported in meta-analyses across diverse tasks (Cabeza andNyberg, 2000; Duncan and Owen, 2000), and finer-grained information about such functionalspecificity should improve the accuracy of “reverse inferences” (Poldrack, 2006) aboutexecutive processes.

In the present study, the best evidence for differences in the neural substrates of the executivefunctions of updating and refreshing comes from a direct contrast between them underconditions where we held other factors (e.g., type of stimuli, control conditions, cue conditions)as similar as possible (Figure 3). It is not surprising that regions more active for updating thanrefreshing included SFJ (often called the frontal eye fields), and areas of bilateral primary andsecondary visual cortex and cuneus. These are regions commonly active in studies of perceptionand perceptual attention, and a primary difference between Update and Refresh conditions wasthat the critical item was perceptually present at the time of Update and not Refresh.Furthermore, SFJ has been associated with maintenance in WM (Courtney et al., 1998;Rothet al, 2006), further supporting the notion that SFJ activity in the Update condition in the presentstudy reflects a change in the state of the WM maintenance network (Roth et al, 2006). In

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addition, a region of right anterior frontal cortex (BA 10) was more active in Update thanRefresh. It has been suggested that anterior frontal cortex (sometimes called frontopolar cortex)is recruited for complex tasks such as those involving monitoring and integrating subgoals(Braver & Bongiolatti, 2002), or contingent task switching or “branching” (Koechlin et al.,1999;Koechlin & Hyafil, 2007). Compared to Refresh, the update task likely involved morecoordination of subgoals given that the task has several components -- reading words whilemaintaining an item in working memory, assessing whether a word matches the maintaineditem, and occasionally replacing the maintained item. Greater activity in right BA 10 couldreflect the simultaneous engagement of multiple, non-superordinate operations, and/orsuspending one operation while another is performed (see Koechlin and Hyafil, 2007).

In the Refresh task participants must reflectively attend to a representation of a word just seenbut no longer present. Prior refresh studies found a network that includes regions similar tothose in the present study that were significantly more active in Refresh than Update: left MFG,left SFG, ACC/MdPFC, and left SMG (Raye et al., 2002; Johnson et al., 2003; Johnson et al.,2004; Johnson et al., 2005; Raye et al., 2007; Raye et al., 2008). Furthermore, studies suggestthat DLPFC and parietal cortex are involved in modulating posterior representational areas(e.g., Johnson and Johnson, 2007), while anterior PFC (BA 10/SFG) is involved in initiatingthe refresh process (Raye et al., 2007, Experiment 1). We found an area of left superior frontalsulcus (largely BA 8, extending into BA 10) in the Refresh > Update contrast. This area wassomewhat posterior and superior to the right BA 10 area where Update was greater thanRefresh. Although these are not exactly homologous areas, these findings may suggest somelateralization of perceptual attention (right PFC) and reflective attention (left PFC). Activityin BA 10 has been hypothesized to be involved in the evaluation of internally generatedinformation (Christoff, Ream, Geddes and Gabrieli, 2003) relative to the evaluation ofinformation in the perceptual environment, and switching between stimulus-oriented andstimulus-independent thought (Gilbert, Frith and Burgess, 2005). In a refresh event in thepresent experiment the participant first sees a cue (stimulus-oriented thought) then mustreactivate a representation of information no longer present (stimulus-independent thought).

Although our focus is on update and refresh, we should note that there were regions of leftventrolateral PFC that were active for maintenance (i.e., maintaining an item in workingmemory in the update task), as would be expected (Smith and Jonides, 1999; see green regionsin Figure 2 and supplementary Table 1). There were very few regions where update, refresh,or both overlapped with areas associated with maintenance, as noted (see supplementary Table1). These findings are consistent with the idea that refresh and update are involved in briefattentional processes that are different from process(es) typically involved in sustaininginformation over intervals of several seconds (see Raye et al., 2007, Exp 2, for additionalevidence differentiating refreshing and rehearsing and Roth et al., 2006, for additional evidencedifferentiating updating from maintenance). Similarly there is a dissociation of regionsinvolved in the sustained vs. transient control of task switching (Braver, Reynolds andDonaldson, 2003). Only a few small regions were responsive to update, refresh andmaintenance. Interestingly, these areas (SMA, middle occipital, and parietal, see Figure 2 andsupplementary Table1) were located directly adjacent to regions active for both update andmaintenance, providing further support that updating involves a change in the state of themaintenance system.

Additional studies involving direct comparison of putatively different executive functions arenecessary to identify the common and distinct regions involved when information enters thecurrent focus of attention, as in studies of perceptual attention (Yantis and Serences, 2003),selection of information via priority changes (Courtney, Roth and Sala, 2007), task updating(Derrfuss et al., 2005), component processes of executive function (e.g., initiating, noting,Johnson et al., 2003; Raye et al., 2007), or shifts in context (Miller and Cohen, 2001;

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MacDonald et al., 2000). Such studies would help disambiguate the functional relevance ofsimilarity and differences in areas activated across experiments, which reflect unspecifiedcombinations of perceptual and reflective attentional demands of complex tasks. That is, suchstudies would clarify the component processes of executive function as discussed in severalmodels (Cowan, 2008; Johnson & Hirst, 1993; Kane and Engle, 2000; Miyake et al, 2001).

ConclusionsThe current results indicate that it is possible to separate executive functioning into regionscommonly active across different executive functions and regions more specific to particularfunctions such as attending to an incoming stimulus to replace a maintained stimulus (update)or attending to an already active representation (refresh). Updating and refreshing are twomechanisms for bringing information into the focus of conscious attention. We would expectthe network of commonly active regions found for updating and refreshing to be found also inwithin-participant comparisons of update or refresh with other tasks requiring changes in whichinformation is currently attended (e.g., visual attention switching, monitoring information inshort term memory or retrieved from long term memory), providing further evidence of asimilarity of function across diverse executive processes. Such studies would also clarifydifferences in executive functions by identifying differences in their neural signatures.

Supplementary MaterialRefer to Web version on PubMed Central for supplementary material.

AcknowledgementsThis research was funded in part by the National Institutes of Health (NS051622 to RTC and AG09253 to MKJ). Theauthors wish to thank Karen Mitchell for comments on the manuscript and the staff of the Yale Magnetic ResonanceResearch Center, especially Hedy Sarofin, Karen Martin and Terry Hickey, for their help with fMRI data acquisition.

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Figure 1.Task design. First participants were cued with the block type, Update or Refresh. In each blockthey read each word. In Update Blocks they were to maintain one word in working memory atall times while reading the stream of words. A row of triangles cued them to update workingmemory by replacing the current contents of working memory with the subsequent word in thestream. (In Update blocks, when they saw a word in the stream that matched the contents ofworking memory they pressed a button.) All Update blocks began with the update cue so thatparticipants immediately maintained an item in working memory. In Refresh Blocks, a row ofdots cued them to think back to the just-previous word. In both block types the control eventwas a row of squares. Participants were instructed to look at the squares and wait for the nextword. Within each block, events occurred pseudorandomly with an Update, Refresh or Controlcue every 3 - 20 seconds (mean time between cues was 10.5 seconds). Each word or cueappeared on the screen for 1 second with a 500 ms inter-stimulus interval containing a visualmask (row of plus signs not shown).

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Figure 2.Overlap analysis of Update, Refresh, and Maintenance (see text). Regions significantlyresponsive to update are shown in orange, refresh in purple and maintenance in green. Regionsresponsive both to update and refresh are shown in red. Regions responsive both to update andmaintenance are shown in yellow. Regions responsive to refresh and maintenance are shownin blue. Regions responsive to update, refresh and maintenance are shown in pink. The leftside of the image represents the left side of the brain.

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Figure 3.Direct comparison of update and refresh. Refresh activity greater than update activity is shownin purple. Update activity greater than refresh activity is shown in orange. The left side of theimage represents the left side of the brain.

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